Abstract

I investigated the role of habitat in shaping mammalian evolution by studying the divergence of two parapatric subspecies, the common brushtail possum, Trichosurus vulpecula vulpecula, and the coppery brushtail possum, T.v.johnsonii, which are found in close proximity on the Atherton Tablelands in North Queensland, Australia. Their reputed distribution and colour differences, then unquantified, suggested that these subspecies may be candidates for evolution through parapatric speciation. This has never before been demonstrated in a mammal.

I discovered that along a habitat gradient from dry sclerophyll forest and mosaic ecotone to rainforest, brushtail possums differed significantly in fur colour. The two morphs were characterised by their fur colour saturation: its colour intensity. Possums with low colour saturation were grey and did not inhabit rainforest. Those with high fur colour saturation were a red-copper colour and did not occur in dry sclerophyll forest. There was a dichotomy in the shade of red expressed among coppery brushtails, which was either a red-orange or redpurple hue, with the different rainforest localities of brushtails significantly associated with this variation. Brushtails in ecotone were either coppery or grey. Fur colour did not vary with distance from the ecotone, nor did fur colour appear to change once established in early development. Ecotone habitats supported very few possums, which may suggest some potential for the ecotone to restrict gene flow along the habitat gradient. The population density in rainforest was 18.6 times that in ecotone, and dry sclerophyll forest supported 8.7 times more brushtails than ecotone habitat.

Coppery and grey brushtail possums were also morphologically distinct in body size. On average, coppery brushtails had ears that were 8mm shorter and 3.4mm thinner, legs that were 3.6mm shorter from knee to heel, and tails 34mm longer than grey brushtail possums of the Atherton Tablelands. There was no sexual dimorphism among brushtail possums along a habitat gradient for body size or colour, suggesting that sexual selection is unlikely to be acting upon these traits to promote divergence.

Comparing mitochondrial DNA control region sequences I found that the morphological distribution was not the result of secondary contact between reciprocally monophyletic populations: coppery and grey possums have evolved together in multiple, distantly related clades. Analyses of the morphology of these clades demonstrated that variation in body-shape morphology was not associated with genetic similarity but with fur colour. As such, possums with the same fur colour also shared body size morphology, whether they were from genetically distant clades or if they were genetically similar. These differences, together with the bimodal distribution of morphs along habitat gradients, indirectly suggested that selection is acting upon these morphological traits to produce the phenotypes and distribution observed.

Examination of the population structure of Atherton Tablelands brushtail possums using mitochondrial DNA control region sequences demonstrated that grouping populations by colour morphology did not explain genetic variation. Genetic differences between populations were not explained by the latitudinal, longitudinal, straight-line or elevation distances between them. However 30.1% of variation could be explained through the identification and separate grouping of the four populations that were closest to rainforest habitat. Along a habitat gradient, grey and coppery populations were distinct.

Investigation of population structure with microsatellite loci showed significant gene flow throughout the Tablelands. Along the habitat gradient, adjacent coppery and grey populations were genetically distinct despite this widespread gene flow. Indeed several geographically more distant populations were not distinct with these markers. This suggested that gene flow is restricted along the habitat gradient. However reproductive isolation was not complete: calculations revealed that gene are exchanged in both directions along the gradient.

Both grey and coppery brushtail possums reproduced synchronously, suggesting that there was no temporal discontinuity to gene flow. However this reproductive synchronicity may limit the potential for polygyny.

With selection acting on morphology and gene flow restricted along a habitat gradient, two possums separated by the same geographic distance should be less related if they are different morphs than if they are the same colour. However, while the pairwise relatedness between different brushtail colour morphs was significantly different to those among coppery brushtails, there was no difference to comparisons among greys. This may be a consequence of the higher population densities of coppery brushtails; relatives may possess smaller home ranges and be closer. However these genetic results did not match our theoretical expectations: possums of different colour morphs and habitats were not less related than possums of the same morph at the same distance of separation. My underlying assumption was that fur colour in the coppery brushtail possum, like so many other species, is a genetically determined trait. If true, then brushtail colour is inherited and determined via an unprecedented mechanism. While this can not be discounted, I questioned my underlying assumption.

Fur colour can also be phenotypically plastic. Climate and diet can determine fur colour, though usually only temporarily. Fur colour did not appear to change once established in early development. The presence and fine-scale distribution of coppery and grey brushtails in rainforest fragments suggested that climatic effects are highly unlikely to be determining fur colour. There has been one previous demonstration of diet permanently determining fur colour via maternal diet acting in utero in laboratory mice. I found that determination of brushtail fur colour by maternal diet and selection upon this trait better explains the observed morphological distribution and genetic structure. Further experimental research is needed to conclusively demonstrate this effect, to explore how widespread this capacity for coppery brushtail colour is, and to discover which foods are involved in fur colour expression. Such an congenital change would be highly significant in evolutionary research as it allows, without mutation, the widespread single generation adaptation of offspring to the environmental conditions experienced by the parent.